Annual Plasmodium falciparum entomological inoculation rates(EIR) across Africa: literature survey, internet access and review

Simon I. Hay1,*, David J. Rogers1, Jonathan F. Toomer1, and Robert W. Snow2,3

1Trypanosomiasis and Land-use in Africa (TALA) Research Group, Department of Zoology,University of Oxford, South Parks Road, Oxford OX1 3PS, UK2Kenya Medical Research Institute/Wellcome Trust Collaborative Programme, P.O. Box 43640,Nairobi, Kenya3Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford,John Radcliffe Hospital, Headington, Oxford OX3 9DS, UK

AbstractThis paper presents the results of an extensive search of the formal and informal literature onannual Plasmodium falciparum entomological inoculation rates (EIR) across Africa from 1980onwards. It first describes how the annual EIR data were collated, summarized, neo-referencedand staged for public access on the internet. Problems of data standardization, reporting accuracyand the subsequent publishing of information on the internet follow. The review was conductedprimarily to investigate the spatial heterogeneity of malaria exposure in Africa and supports theidea of highly heterogeneous risk at the continental, regional and country levels. The implicationsfor malaria control of the significant spatial (and seasonal) variation in exposure to infectedmosquito bites are discussed.

Keywordsmalaria; Plasmodium fulciparum; entomological inoculation rate (EIR); biting rate; sporozoiteindex; transmission; disease control; Africa

IntroductionMalaria continues to pose a major public-health threat to many countries in Africa (Snow etal., 1999a). The launch of Roll Back Malaria (RBM) (Nabarro & Tayler, 1998; WHO, 1998)therefore was regarded as timely by many. International public health initiatives such asRBM, aimed at reducing continental burdens of malaria, require an understanding ofcontemporary malaria distribution, risk and burden (Snow et al., 1996; Le Sueur et al., 1997,Snow et al., 1998a). Several attempts have been made to explore continental malariadistribution (Sutherst, 1993; Lindsay & Martens, 1998; Lindsay et al., 1998; Craig et al.,1999) and disease burden (Snow et al., 1999a, 1999b) using climate models andmalariometric data gathered from the literature. There is increasing evidence, however, thatthe relationship between the frequency of infection and disease outcome is complex andcontrol options should be selected accordingly (Snow et al., 1997, 1998b; Snow & Marsh,1998: Gupta et al., 1999a, 1999b).

*Author for correspondence: phone +44 (0) 1865 271243, fax +44 (0) 1865 271243, simon.hay@zoo.ox.ac.uk.

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Published in final edited form as:Trans R Soc Trop Med Hyg. 2000 ; 94(2): 113–127.

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In the absence of a comprehensive reference on malaria exposure in Africa, and owing to itsimportance in international efforts in malaria control, an overview of the availableentomological evidence describing the average annual risk across Africa of receiving aPlasmodium falciparum infected bite from the local vector population [the annualentomological inoculation rate (EIR)] was initiated. This review focuses particularly on thespatial heterogeneity of annual EIR within Africa and its implications for the rationalizationof malaria control. A discussion of some of the methodological difficulties involved incomparing annual EIR information is also provided. There is further consideration of thelimitations and benefits of data-sharing over the internet. The data described were predictedfor non-surveyed areas using remotely sensed imagery from meteorological satellites (D. J.Rogers et al., paper in preparation), to provide the first annual EIR surfaces for the Africancontinent.

Materials and MethodsAnnual EIR definition

The activity of the anopheline vector of malaria provides the basis for calculating the EIR,h’, the daily number of infective mosquito bites received per person (MacDonald, 1957).Algebraically h’ = mas; where m is the anopheline density in relation to humans; a is theaverage number of persons bitten by 1 mosquito in a day, and s is the proportion ofmosquitoes with sporozoites in their salivary glands. It is obvious that if the EIR value is tobe representative of the year, the estimates of the biting rate and the sporozoite index mustbe repeated at a monthly (or higher) frequency, for at least a year or complete transmissionseason. The annual EIR is a favoured measure for assessing malaria endemicity (Burkot &Graves, 1995) and thus the suitability of vector control (Coosemans et al., 1992), as well asthe risk of epidemic development (Onori & Grab, 1980). Measuring the annual EIR presentsseveral major difficulties, however, since the entomological methods used in its estimationhave not been standardized (Githeko et al., 1996).

Human biting rateThe most direct way to measure the human biting rate (the product of ma) is the human baitcatch (WHO, 1975). This involves a team waiting in a given location, usually throughout thenight, collecting all the mosquitoes that attempt to feed on exposed individuals. Despitebeing expensive, technically difficult to replicate and unethical in areas of drug-resistantmalaria, this method is unique in that it directly samples human-biting mosquitoes (Le Goffet al., 1997). Other sampling methods such as pyrethrum spray collections and light and exittraps depend on mosquito behaviours that are less directly associated with feeding onhumans (Garret-Jones, 1970; Service, 1993). Fortunately, the sampling biases between themost commonly used techniques, human bait and light traps, have been investigated (Lineset al., 1991; Faye et al., 1992; Mbogo et al., 1993a; Davis et al., 1995; Smith, 1995).Correction factors have also been suggested to account for children experiencing lowerbiting rates than adults in the same location (Port et al., 1980). Details of the protocol usedfor the standardization of data are presented below.

Sporozoite indexMeasurements of the sporozoite index (s) require the number of infective mosquitoes (thosewith sporozoites in their salivary glands) in the local population to be determined (WHO,1975). Ideally, but not always, the sporozoite index is derived from the biting rate sample.The traditional method was to dissect all sampled mosquitoes for their salivary glands andsubject them to procedures designed to help reveal potential sporozoites under themicroscope. More recently, the enzyme-linked immunosorbent assay (ELISA) techniques,which detect Plasmodium-specific circumsporozoite antigens from mosquito head and/or

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thorax samples, are being increasingly used owing to their greater sensitivity and speciesspecificity (Burkot et al., 1984). No attempt was made to standardize the sporozoite index inthis study because sensitivity and specificity of microscopy (Kilian et al., 2000) and ELISAtechniques will vary between studies.

Identification of sources of annual EIR dataOnline abstracting databases (Biological Abstracts®, BIOSIS, Philadelphia, Pennsylvania,USA, MEDLINE®, US National Library of Medicine, Bethesda, Maryland, USA; CABHEALTH, CAB International Inc., Wallingford, Oxfordshire, UK; and the ZoologicalRecord Online®, BIOSIS, Philadelphia, Pennsylvania, USA) were searched with thefollowing keywords (entomological inoculation rate, EIR, h’, biting rate, ma, sporozoiteindex, s, Plasmodium falciparum Anopheles gambiae, Anopheles funestus, Anopheles,vectorial capacity, malaria transmission, malaria control, bednets, ITBN, human bait,pyrethroid spray, light trap, exit trap, bionomics). This search resulted in a large number ofreferences which were scrutinized for annual EIR data. From this subset of publications a‘key author list’ was compiled and these names were re-entered into the abstractingdatabases and further relevant manuscripts were retrieved. The bibliographies of allrecovered manuscripts were then checked for potential additional references. Thesereferences were collected and the searching strategies repeated until no new information wasforthcoming. The list of papers found for each author was then compiled and a letter sent toeach individual requesting they check that the bibliography was complete and the data wereabstracted correctly. Forty-three letters were sent, to which there were 21 replies, mostlywith further information from the ‘grey’ literature.

Recording and standardization of the annual EIR valuesThe values recorded in Table 1 are P. falciparum-infected bites per adult, per night indoors,using human biting rates averaged over a year. In most studies the author(s) had expressedtheir data in the above format. When adjustment was necessary, this commonly involvedconverting light-trap catches to their human-bait equivalent by multiplying by 1·5 (Lines etal., 1991) and more rarely converting child EIR values to those of adults by multiplying by3·57 (Port et al., 1980). In addition to the annual EIR, the average annual biting rate and thesporozoite index are also presented. It should be noted, however, that owing to theapproximation inherent in rounding, the product of the biting and sporozoite indices may notexactly match the recorded annual EIR. For each location an index of the length of thetransmission season was expressed as the number of months in which 75% of the annualEIR was transmitted. When studies did not provide enough information for this to becalculated the length of the transmission season only was recorded. The percentage of thetotal annual EIR transmitted by Anopheles gambiae s.l. freshwater species, An. funestus andall other species was also noted. Finally, the land-use in which the study site was locatedwas classified as dominantly rural, irrigated rice or urban.

Criteria for data exclusionAnnual EIR data measured before 1980 were excluded because it was not clear whetherinformation collected over 20 years ago would be representative of the conditions today. Inaddition, the data were also extracted for comparison with contemporaneous meteorologicalsatellite sensor data available from 1981 to date (D. J. Rogers et al., paper in preparation).Moreover, data before 1980 were more difficult to search using electronic abstractingdatabases, although such information would make a useful addition to those compiled here.Sites were also excluded if malaria control activities, local bednet and/or insecticide usagewere reported. The possibility of unreported use of bednets, insecticide and repellents in thestudies remains a problem, however, so these data are best interpreted as potential EIRvalues. Finally, data were not included if the sampling frequency and duration of

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observation were insufficient to record the EIR throughout the entire year or transmissionseason.

Methodological informationEIR sampling methods vary considerably and those used in obtaining the biting rate (humanbait, pyrethroid spraying, light or exit traps) and the means of measuring the sporozoiteindex (dissection or ELISA) are noted in Table 1. Calculation of the sporozoite index wasoften complicated by the subdivision of the index into proportions due to differentPlasmodium species. Only the sporozoite indices attributable to P. falciparum were used.Where the relative contribution to total transmission level for each species was notdocumented, the total was assumed to be due to P. falciparum.

Geo-referencingSites were geo-referenced using information from the original references, published mapsand/or the GeoName™ digital gazetteer CD-ROM (GDE Systems Inc., San Diego, CA,USA). Sites for which co-ordinates were found are included in Table 1. Those sites whichhad conflicting latitude and longitude values from different sources were double-checkedand the erroneous co-ordinates discarded. The method used to geo-reference each annualEIR value was therefore also recorded.

Data distributionThe information reviewed in this paper is available for downloading from both the Mappingmalaria risk in Africa/Atlas du risque de la malaria en Afrique (MARA/ARMA URL; http://www.mara.org.za) and Scientists for Health And REsearch for Development (SHAREDURL; http://www.shared.de) web sites as comma separated text files. Mechanisms forcorrecting existing and adding additional information will be staged in the near future. TheAppendix, which provides an example of a completed data sheet used to abstract data in thisstudy, is also available for downloading.

ResultsAnnual EIR data

Four hundred references were retrieved and searched for annual EIR data of which 91satisfied the selection criteria. These papers contained 201 temporally distinct annual EIRmeasurements from 16 countries. Of these, 159 were spatially distinct. Table 1 contains allthe 193 geo-registered sites from 15 countries with data collected after 1980. Table 2contains annual EIR data that could not be geo-registered: 8 sites in 5 countries. The Figureshows the distribution of the study sites detailed in Table 1. The apparent disparity in thenumber of sites is due to the close proximity of many studies which could not be resolved ona map of Africa at the continental scale.

These studies collectively demonstrate that Africa has substantial cross-continent variabilityin annual EIR. The mean annual EIR value for the 159 spatially distinct sites was 121infected bites per annum, although exposure ranged from a maximum of 884 to a minimumof 0. The local land-use also had a major effect on annual EIR. The ‘rural’ class had anoverall mean of 146 (ranae 0–884) while those surrounded by irrigated rice were lessexposed with a mean of 99 (range 0–601) and those in urban areas receiving significantlylower exposure with a mean of 14 (range 0–43). The variance in annual EIR expressed asthe [(standard error/mean) × 100] is shown by country in Table 3. Spatially distinct ruralsites only (n = 133) were used, to help control for major agricultural or demographic impact,and only countries with at least 10 spatially distinct study sites were included. Tanzaniashowed the least variance at 10·9%, and Senegal the highest at 42%. Finally, of the 133 sites

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for which seasonality information could be gathered, 30% showed acute seasonal variationin annual EIR (i.e., with 75% of annual transmission occurring in 1–3 months).

Study methodologyBiting rates were determined primarily by human-bait samples (n = 111), followed by light-traps (n = 31), pyrethrum spray-catches (n = 22) and exit-traps (n = 2) measurements.Combinations of the above techniques were used in 17 studies, whilst 18 more provided noinformation on how the biting rate estimate was obtained. The methods used to evaluate thesporozoite index were roughly even, with 82 determined by dissection and 99 by ELISA.Three records were calculated using the average of dissection and ELISA and 17 did notrecord the methodology used.

Geo-referencingThree of the 201 annual EIR values were published with an accurate latitude and longitudeof the study area. Correspondence with authors provided co-ordinate details for a further 33sites. The largest source of geo-referencing information was obtained from the GeoName™digital gazetteer CD-ROM which geo-referenced 100 annual EIR values. Finally, publishedmaps were used to uncover the co-ordinates of a further 57 sites. This left the 8 unlocatedstudy sites shown in Table 2.

DiscussionAnnual EIR heterogeneity

It has been observed that Africa can support a very wide range of EIRs (Gilles, 1993). Morerecently, however, variation in infection risk has been linked to very different clinicalpatterns and public health burdens (Snow et al., 1997, 1998b; Snow & Marsh, 1998; Guptaet al., 1999a, 1999b). Although this study cannot claim to have identified every study ofestimated annual EIR in Africa since 1980, the results of the search do support the claim fora diverse transmission pattern for the continent. Of particular interest in this respect is theenormous apparent variation within countries such as Senegal and Kenya. If this variationreflects sub-regional ecological heterogeneity, rather than sampling biases in the distributionof studies, it has important implications for disease management.

The results demonstrate a marked demographic influence on annual EIR values. Therelatively small annual EIR in urban versus rural settings was not unexpected and isexemplified in the series of studies around Brazzaville in The Congo (Trape & Zoulani,1987b) and neighbouring Kinshasa in Zaire (Coene, 1993). The impact of irrigated ricefarming on surrounding EIRs is complicated. It has been shown to increase (Coosemans,1985), have little overall effect upon (Robert et al., 1985; Githeko et al., 1993; Dossou-yovoet al., 1994) and also decrease (Robert et al., 1985; Githeko et al., 1993; Dossou-yovo et al.,1994) malaria transmission depending on the location. This variation can be due to manyfactors, such as relative effects of irrigation on species abundance and sporozoite rate, thenumber of rice harvests, surrounding human population numbers and levels of breeding sitecontamination, the number of cattle in the locality, as well as the degree of local immunity.The data collated here are insufficient to explore any of these mechanisms in detail, but it isinteresting to note that when populations near irrigated rice areas were compared to thosefrom the sample of rural Africa as a whole they were, on average, less exposed.

Year-to-year variation in annual EIR is also very important, particularly in naturallyseasonal areas. Too few investigations published data over multiple years, however, to makereliable generalizations. The following studies from Senegal should be considered wheninterpreting single annual EIR estimates from a site, since the annual EIR ranged from 89 to

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238 in Dielmo over a 3-year monitoring period (Fontenille et al., 1997b) and from 7 to 63infected bites per year over a 4-year monitoring period in Ndiop (Fontenille et al., 1997a).

The Figure shows that entomological studies are preferentially conducted where malaria isknown to exist and is often a recognized local health problem. For example, the range ofestimates for Burundi (Coosemans, 1985; Van Bortel et al., 1996) suggests a country ofintense transmission, whilst most of Burundi is at high altitude and free from malaria (Vander Stuyft et al., 1993). The Figure also shows that studies are more likely to be conductedin locations where malaria research has a strong historical basis. In Kenya, for example, thesites for most data neighbour the Kenyan Medical Research Institute (KEMRI) researchcentres on the coast and Lake Victoria. The annual EIR statistics presented for each countrymust therefore be interpreted with this caveat. It would also be of value if an internationalnetwork could be developed to map EIR using standardized methods in a grid-based systemacross Africa to record more closely the spatial distribution of malaria transmission on thecontinent, rather than the distribution of medical research centres and their accessible fieldsites.

Information technology issuesThe data presented in Table 1 have been staged on the internet for public access (seeMaterials and Methods) along with predicted maps of annual EIR for the African continent(D. J. Rogers et al., paper in preparation). This follows an objective to initiate the provisionof web-based information to guide malaria control by the year 2000 (MARA/ARMA, 1998).There is a growing emphasis in many sectors on the potential benefits of the rapid internet-based supply of quality information. The greatest value of this increased information flowshould be the possibility for iterative information updates with new, missed or correctedinformation. The most obvious problems to resolve are those of data-quality control and theprovision of information in a manner accessible to a variety of users. The range of issuespertaining to data supply for malaria control planning is far from being resolved and is notappropriately addressed in this article. The authors have simply sought to make informationavailable that might be of use to those collating data on malaria risk. Furthermore, these dataare presented in such a way that those who may take issue with the protocol adopted canconsult the original sources at the internet sites specified in Materials and Methods.

Data quality issuesIt is evident that considerable resources have been expended by researchers, institutes anddonors to provide annual EIR information across a range of sites in Africa over the past 2decades. One of the major problems involved in comparing this information is the absenceof data standardization between studies. An attempt has been made in this paper to highlightthese issues.

The second major problem relates to the comprehensiveness of the reporting of annual EIRinformation. Most studies were incomplete in the range of information recorded. Similarproblems have been experienced in parallel exercises to collate parasite rate (MARA/ARMA, 1998) and helminth infection data (Brooker et al., 2000) in Africa. The followingdata are suggested as the minimum requirement for future peer-reviewed reporting of annualEIR. First, all methodological information should be identified including exactly how, whenand for what duration biting rate and sporozoite indices were determined. It is also importantthat accurate names and co-ordinates are given for each of the study sites. Brief details aboutthe nature of the surrounding land-use are useful in the determination of the extent ofagricultural and demographic impacts. Where ELISA techniques are used it is helpful torecord the proportion of infective bites that can be attributed to each Plasmodium speciesand the vector species by which malaria is locally transmitted. If future reporting completed

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the list of information indicated in the Appendix, the foundation for a centralized, high-quality information database of annual EIR estimates across Africa would be assured.

The third problem is that, since accurate measurement of the EIR is labour intensive andthereby costly, estimates are spatially and temporally infrequent and unavailable for manysettings. Another part of the study attempted to overcome this paucity of ground data bypredicting annual EIR values across Africa using the information reviewed here andenvironmental data derived from meteorological satellite sensors (D. J. Rogers et al., paperin preparation).

Reviews are becoming increasingly important within the arena of evidence-based planningfor disease control and prevention (Bero & Rennie, 1995; Bero, 1996). Furthermore,improved internet access will facilitate the use of central data resources by a wider spectrumof the research and control community. It is hoped the presentation and synthesis of workhere, and in the public domain, will expedite future information gathering required forrationalization of malaria control in space and time.

AcknowledgmentsThe following people provided substantial help in both the search for and assessment of the accuracy of theinformation presented in this review: John Beier, Pierre Carnevale, José Coene, Chris Curtis, Pierre Fontenille,Pierre Gazin, Andrew Githeko, S. Karch, Steve Lindsay, L. Manga, Louis Molineaux, Jean Mouchet, EskildPetersen, J. Pull, Vincent Robert, Clive Shiff, Tom Smith, Marcel Tanner, Emanuel Temu, Madeleine Thompsonand Peter Trigg. All remaining errors are entirely the responsibility of the authors. We are grateful to Joseph Lines,David Kelly, Bill Snow and Mike Packer for their comments on the manuscript. We thank the Sir Halley StewartTrust for providing salary support to J.F.T. This publication is also an output from a research project funded by theDepartment for International Development (DFID) of the UK, project ZC0012. However, the DFID can accept noresponsibility for any information provided, or views expressed. S.I.H. is an Advanced Training Fellow with theWellcome Trust (#056642). R.W.S. is a senior Wellcome Trust Fellow in Basic Biomedical Sciences (#033340).

Appendix

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Figure.A map showing the geo-referenced locations in Africa for which annual EIR data werepublished. The top left corner is 40°N, 20°W. Each grid square is 5 × 5 degrees and north isto the top of the page.

Hay et al. Page 16

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Hay et al. Page 17

Tabl

e 1

Geo

-ref

eren

ced

loca

tions

in A

fric

a fo

r w

hich

ann

ual P

. fal

cipa

rum

EIR

dat

a w

ere

publ

ishe

d

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

Ben

in

C

oton

ou, G

béga

mé

quar

ter

2·45

, 6·3

6aU

Jan

1987

–Dec

198

72·

80e

1179

g33

·01

100:

0:0

Ako

gbet

o et

al.,

199

2

C

oton

ou, L

adji

quar

ter

2·43

, 6·3

8aR

Jan

1987

–Dec

198

71·

60e

3666

g58

·04

100:

0:0

Ako

gbet

o et

al.,

199

2

C

oton

ou, S

aint

e-R

ita

N

orde

qua

rter

2·42

, 6·3

7aR

Jan

1987

–Dec

198

71·

40e

3363

g47

.04

100:

0:0

Ako

gbet

o et

al.,

199

2

G

anvi

é2·

42, 6

·47b

RJa

n 19

93–D

ec 1

993

0·43

e25

55g

11·0

6P:

A:P

Ako

gbet

o, 1

995

G

anvi

é, n

ear

lake

Nok

oué

2·42

, 6·4

2aR

Jan

1993

–Dec

199

50·

37 e

2917

g10

·86

100:

0:0

Ako

gbet

o &

Nah

um, 1

996

Bur

kina

Fas

o

B

arna

−4·

42, 1

1·38

bR

Jan

1981

–Dec

198

1N

AN

AN

AN

A17

5·2

357

:35:

8C

arne

vale

& R

ober

t, 19

87

B

aré

−4·

10, 1

1·08

bR

Jan

1981

–Dec

198

1N

AN

AN

AN

A91

·33

57:3

5:8

Car

neva

le &

Rob

ert,

1987

B

arko

urnb

ilen

and

Bar

koun

doub

a−

1·23

, 12·

67b

RA

ug 1

994–

Jun

1995

NA

fN

Ah

140·

04–

5P

:P:A

Mod

iano

et a

l., 1

996

B

obo-

Dio

ulas

so−

4·30

, 11·

20b

UN

ov 1

991–

Jan

1993

0·10

e21

50g

2·2

NA

100:

0:0

Loc

houa

rn &

Gaz

in, 1

993

B

obo-

Dio

ulas

so, C

olrn

a-

N

ord

quar

ter

−4·

30, 1

1·21

aU

/RJa

n 19

85–D

ec 1

985

0·19

e24

21 g

4·6

NA

100:

0:0

Rob

ert e

t al.,

198

6

B

obo-

Dio

ulas

so,

Dia

rado

ugou

qua

rter

−4·

29, 1

1·18

aU

Jan

1985

–Dec

198

50·

19e

74 g

0·1

NA

100:

0:0

Rob

ert e

t al.,

198

6

B

obo-

Dio

ulas

so,

Dio

ulas

soba

qua

rter

−4·

30, 1

1·19

aU

Jan

1985

–Dec

198

50·

19e

289

g0·

6N

A10

0:0:

0R

ober

t et a

l., 1

986

B

obo-

Dio

ulas

so, S

arfa

lao

quar

ter

−4·

30, 1

1·20

bU

Jun

1993

–Sep

199

30·

50e

800

g4·

0N

A10

0:0:

0G

azin

et a

l., 1

996

D

andé

and

Tag

o−

4·55

, 11·

59a

RJa

n 19

83–D

ec 1

984

3·99

e13

80g

55·0

369

:31:

0R

ober

t et a

l., 1

985

D

esso

−4·

28, 1

1·35

bR

Jan

1981

–Dec

198

1N

AN

AN

AN

A20

8·1

357

:35:

8C

arne

vale

& R

ober

t, 19

87

G

oung

hin

Nor

d−

1·55

, 12·

37a

UJu

l 198

4–D

ec 1

984

NA

eN

Ah

0·0

00:

0:0

Ros

si e

t al.,

198

6

K

aran

gass

o−

4·63

, 11·

22b

RJa

n 19

85–F

eb 1

986

4·13

f63

60g

262·

84

57:4

1:2*

Bou

din

et a

l., 1

991

K

aran

gass

o, K

oko

subu

rb−

4·65

, 11·

22a

RFe

b 19

85–F

eb 1

986

NA

eN

Ag

116.

04

P:P:

PR

ober

t et a

l., 1

988

K

aran

gass

o, K

oko

subu

rb−

4·65

, 11·

22a

RM

ay 1

985–

Apr

198

62·

60 e

4548

g11

6·1

551

:49:

0C

arne

vale

et a

l., 1

988

K

aran

gass

o, K

oko

subu

rb−

4·65

, 11·

22a

RM

ay 1

986–

Apr

198

74·

56 e

4913

g22

3·8

459

:41:

0C

arne

vale

et a

l., 1

988

K

aran

gass

o, M

assa

sso

subu

rb−

4·64

, 11·

21a

RFe

b 19

85–F

eb 1

986

NA

eN

Ag

370·

04

P:P:

PR

ober

t et a

l., 1

988

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Hay et al. Page 18

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

K

aran

gass

o, M

assa

sso

subu

rb−

4.64

, 11.

21a

RM

ay 1

985–

Apr

198

65·

75 e

7012

g40

3·3

460

:37:

3C

arne

vale

et a

l., 1

988

K

ongo

djan

−4·

45, 1

1·58

aR

Jan

1983

–Dec

198

41·

78 e

7480

g13

3·0

452

:48:

0R

ober

t et a

l., 1

985

K

ongo

djan

−4·

45, 1

1·58

aR

Jan

1983

–Dec

198

3N

Ae

NA

g13

3·0

3P:

P:A

Gaz

in e

t al.,

198

8

K

oro

−4·

20, 1

1·15

bR

Jan

1981

–Dec

198

1N

AN

AN

AN

A17

1·6

357

:35:

8C

arne

vale

& R

ober

t, 19

87

K

oubr

i−

1·38

, 12·

15a

RJu

l 198

4–D

ec 1

984

NA

eN

Ah

441·

63

P:P:

AR

ossi

et a

l., 1

986

O

uaga

doug

ou, K

olog

h

N

aba

subu

rb−

1·54

, 12·

39a

UJu

l 198

4–D

ec 1

984

NA

eN

Ah

1·5

3P:

P:A

Ros

si e

t al.,

198

6

O

uaga

doug

ou,

Non

grem

assm

sub

urb

−1·

51, 1

2·40

aU

Jul 1

984–

Dec

198

4N

Ac

NA

h7·

73

P:P:

AR

ossi

et a

l., 1

986

O

uaga

doug

ou,

Sain

t Cam

ille

subu

rb−

1·52

, 12·

36a

UJu

l 198

4–D

ec 1

984

NA

eN

Ah

5·6

1P:

P:A

Ros

si e

t al.,

198

6

O

uaga

doug

ou, S

aint

Léo

n

su

burb

−1·

52, 1

2·37

aU

Jul 1

984–

Dec

198

4N

Ae

NA

h0·

00

0:0:

0R

ossi

et a

l., 1

986

Pa

bré

−1·

58, 1

2·50

aR

Jul 1

984–

Dec

198

4N

Ae

NA

h11

3·0

3P:

P:A

Ros

si e

t al.,

198

6

So

umos

so−

4·05

, 11·

02a

RJa

n 19

81–D

ec 1

981

NA

NA

NA

NA

200·

83

57:3

5:8

Car

neva

le &

Rob

ert,

1987

T

ago

−4·

38, 1

1·67

aR

Jan

1983

–Dec

198

3N

Ae

NA

g82

·03

P:P:

AG

azin

et a

l., 1

988

T

ouko

ro−

4·25

, 11·

43b

RJa

n 19

81–D

ec 1

981

NA

NA

NA

NA

76·7

357

:35:

8C

arne

vale

& R

ober

t, 19

87

V

K1

−4·

41, 1

1·35

aI

Jan

1981

–Dec

198

1N

AN

AN

AN

A0

372

:25:

3C

arne

vale

& R

ober

t, 19

87

V

K2

−4·

41, 1

1·37

aI

Jan

1981

–Dec

198

1N

AN

AN

AN

A21

·93

72:2

5:3

Car

neva

le &

Rob

ert,

1987

V

K3

−4·

41, 1

1·38

aI

Jan

1981

–Dec

198

1N

AN

AN

AN

A62

·13

72:2

5:3

Car

neva

le &

Rob

ert,

1987

V

K4

−4·

42, 1

1·37

aI

Jan

1981

–Dec

198

1N

AN

AN

AN

A20

·13

72:2

5:3

Car

neva

le &

Rob

ert,

1987

V

K4

−4·

42, 1

1·37

aI

Jan

1983

–Dec

198

40.

36 e

1400

0g50

·04

100:

0:0

Rob

ert e

t al.,

198

5

V

K4

−4·

42, 1

1·37

aI

May

198

5–A

pr 1

986

0–21

e25

857g

54·9

490

:10:

0R

ober

t & C

arne

vale

, 199

1

V

K5

−4·

43, 1

1·38

aI

Jan

1981

–Dec

198

1N

AN

AN

AN

A36

·53

72:2

5:3

Car

neva

le &

Rob

ert,

1987

V

K6

−4·

44, 1

1·37

aI

Jan

1981

–Dec

198

1N

AN

AN

AN

A54

·83

72:2

5:3

Car

neva

le &

Rob

ert,

1987

V

K6

−4·

44, 1

1·37

aI

Jan

1983

–Dec

198

40–

43 e

1390

0g60

·02

90:1

0:0

Rob

ert e

t al.,

198

5

Z

agto

uli

−1·

63, 1

2·33

aR

/IJu

l 198

4–D

ec19

84N

Ae

NA

h82

2P:

P:A

Ros

si e

t al.,

198

6

Bur

undi

G

asan

ge29

·60,

−4,

32a

NA

Nov

199

2–0c

t 199

33·

14 e

8503

g26

7·0

6P:

P:A

Van

Bor

tel e

t al.,

199

6

G

ihan

ga M

ulir

a29

·29,

−3·

19b

IJa

n 19

83–D

ec 1

983

0·48

e21

499g

103·

212

96:4

:0C

oose

man

s, 1

985

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Hay et al. Page 19

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

G

isen

ga29

·67,

−4,

44a

NA

Nov

199

2–M

ay 1

994

3·85

e65

34 g

251·

75

P:P:

AV

an B

orte

l et a

l., 1

996

K

azir

abag

eni

29·6

3, −

4·23

aR

Nov

199

2–M

ay 1

994

2·02

e17

53 g

35·4

5P:

P:A

Van

Bor

tel e

t al.,

199

6

M

uger

e29

·66,

−4,

37a

IN

ov 1

992–

0ct 1

993

1–02

e59

021

g60

0·9

7P:

P:A

Van

Bor

tel e

t al.,

199

6

Cam

eroo

n

E

bogo

11·4

7, 3

·40b

RA

pr 1

991–

Mar

199

20·

93 e

3818

9g35

5·0

614

:0:8

6N

jan

Nlo

ga e

t al.,

199

3

E

dea,

Bili

lang

sub

urb

10·1

3, 3

·80a

UJa

n 19

90–D

ec 1

990

1·20

e31

9g3·

8N

A10

0:0:

0R

ober

t et a

l., 1

993

E

dea,

Pon

go s

ubur

b10

·13,

3·8

0aU

Jan

1990

–Dec

199

08·

21 e

368g

30·2

NA

100:

0:0

Man

ga e

t al.,

199

3

E

toa

11·4

8, 3

·77b

RFe

b 19

96–M

ay 1

996

4·10

e11

571g

474·

5N

AP:

55:4

5M

anga

et a

l., 1

997b

M

bébé

11·0

0, 4

·15a

RA

pr 1

989–

Mar

199

01–

93 N

A10

330g

200·

05

36:9

:55

Le

Gof

f et

al.,

199

2

N

dita

m11

·26,

5·3

6aR

May

199

5–M

ar 1

996

9·40

e87

6g82

·11

100:

0:0

Man

ga e

t al.,

199

7a

N

sim

alen

, Eko

ko12

·12,

3·8

2aR

Apr

199

1–M

ar 1

992

1·22

e87

24g

106·

05–

613

:0:8

7M

anga

et a

l., 1

995

N

sim

alen

, Nko

l Mef

ou11

·57,

3·7

0aR

Apr

199

1–M

ar 1

993

2·33

e29

20g

68·0

610

0:0:

0M

anga

et a

l., 1

995

Sa

naga

riv

er v

illag

es11

·00,

4·1

5aR

Apr

198

9–M

ar 1

990

1·77

e10

303g

182·

16

43:0

:57

Car

neva

le e

t al.,

199

2

Y

aoun

dé, E

ssos

11·0

0, 3

·00a

UM

ar 1

989–

Feb

1990

20·3

e64

g13

·0N

A10

0:0:

0M

anga

et a

l., 1

993

Y

aoun

dé, N

kol B

ikok

quar

ter

11·5

2, 3

·87a

UM

ar 1

989–

Mar

199

05·

00e

284·

7g14

·21

100:

0:0

Fond

jo e

t al.,

199

2

Con

go, D

emoc

ratic

Rep

ublic

of

K

inko

lé15

·51,

−4·

36a

RFe

b 19

90–D

ec 1

991

3·24

e12

41g

40·2

1210

0:0:

0K

arch

et a

l., 1

993

K

insh

asa,

Kim

bang

u 3

dist

rict

15·3

1, −

4, 3

5·c

USe

p 19

88–D

ec 1

989

1·86

f18

62 g

29·2

5–6

100:

0:0

Coe

ne, 1

993

K

insh

asa,

Kw

amut

hu

di

stri

ct15

·27,

−4,

46c

RSe

p 19

88–D

ec 1

989

7·41

f61

32 g

454·

45–

686

:2:1

2C

oene

, 199

3

K

insh

asa,

rur

al a

rea

15·3

0, −

4·44

aR

Apr

198

9–0c

t 199

0N

Ae

NA

g61

2·0

NA

100:

0:0

Kar

ch e

t al.,

199

2

K

insh

asa,

sem

i–ru

ral a

rea

15·3

5, −

4·36

aR

/UA

pr 1

989–

0ct 1

990

NA

eN

Ag

198.

7N

A10

0:0:

0K

arch

et a

l., 1

992

K

insh

asa,

urb

an a

rea

15·3

1, −

4·31

aU

Apr

198

9–O

ct 1

990

0·3e

953g

2·8

NA

100:

0:0

Kar

ch e

t al.,

199

2

Con

go, R

epub

lic o

f

B

razz

avill

e15

·28,

−4·

26b

UO

ct 1

982–

May

198

43·

47e

650g

22·5

NA

100:

0:0

Tra

pe &

Zou

lani

, 198

7b

K

ulila

12·4

3, −

4·17

aR

Oct

198

1–O

ct 1

982

4·91

e81

03 g

397·

95

97:3

:0R

icha

rd e

t al.,

198

8

L

inzo

lo15

·11,

−4·

41 b

RO

ct 1

981–

Jan

1984

2·11

e11

673g

246·

09

NA

Tra

pe &

Zou

lani

, 198

7a

Trans R Soc Trop Med Hyg. Author manuscript; available in PMC 2011 October 31.

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C Funders A

uthor Manuscripts

Europe PM

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uthor Manuscripts

Hay et al. Page 20

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

L

inzo

lo15

·11,

−4·

41 b

RO

ct 1

983–

Sep

1984

NA

NA

NN

g23

4·6

996

:4:0

Tra

pe e

t al.,

198

7

M

akab

a12

·38,

−4·

14b

RO

ct 1

981–

0ct 1

982

6·85

e11

68 g

80·0

689

:11:

0R

icha

rd e

t al.,

198

8

Côt

e d’

Ivoi

re

A

llouk

oukr

o−

5·08

, 7·8

0aR

Jan

1991

–Dec

199

13·

13 e

8507

g26

6·5

677

:23:

0D

osso

u-yo

vo e

t al.,

199

5

A

llouk

oukr

o−

5·08

, 7·8

0aR

Jan

1992

–Dec

199

23·

39 e

5792

g19

6·5

581

:19:

0D

osso

u-yo

vo e

t al.,

199

5

Egy

pt

E

l Zaw

ya30

·85,

29·

42a

RFe

b 19

83–F

eb 1

984

0·00

e12

8g0·

00

0:0:

0E

l Sai

d et

al.,

198

6

Gam

bia,

The

B

akau

−16

·68,

13·

48b

UJu

n 19

88–M

ay 1

989

0·98

f12

8g1·

0 k

NA

100:

0:0

Lin

dsay

et a

l., 1

990

B

arok

unda

−15

·32,

13·

65b

RN

A 1

988–

NA

198

82·

97 f

3701

i11

0·0

510

0:0:

0L

inds

ay e

t al.,

199

3

B

iran

Gid

do Y

a−

15·8

5, 1

3·59

aR

Jun

1986

–Dec

198

62·

67 e

412j

11·0

310

0:0:

0L

inds

ay e

t al.,

198

9

B

wia

m−

16·0

9, 1

3·23

cR

Jan

1991

–Dec

199

12.

47f

37h

0·9

5P:

A:P

Tho

mso

n et

al.,

199

4

D

asila

mia

−14

·27,

13·

41 c

RJa

n 19

91–D

ec 1

991

2·23

f54

h1·

25

P:A

:PT

hom

son

et a

l., 1

994

D

asila

mib

−15

·23,

13·

48b

RN

A 1

988–

NA

198

81·

29 f

1160

i15

·05

100:

0:0

Lin

dsay

et a

l., 1

993

D

ongo

ro B

a−

15·2

8, 1

3·38

bR

NA

198

8–N

A 1

988

17·8

6 f

448i

80·0

510

0:0:

0L

inds

ay e

t al.,

199

3

Ja

hally

−14

·97,

13·

55c

RJa

n 19

91–D

ec 1

991

0·95

f44

3h4·

25

P:A

:PT

hom

son

et a

l., 1

995

Ja

lang

bere

h−

15·4

0, 1

3·38

bR

NA

198

8–N

A 1

988

9·10

f76

9i70

·05

100:

0:0

Lin

dsay

et a

l., 1

993

Je

ssad

i−

15·3

0, 1

3·63

bR

NA

198

8–N

A 1

988

2·69

f23

80i

64·0

510

0:0:

0L

inds

ay e

t al.,

199

3

K

atam

ina

−15

·28,

13·

55b

RN

A 1

988–

NA

198

80·

37 f

1076

i4·

05

100:

0:0

Lin

dsay

et a

l., 1

993

K

erew

an−

16·

09, 1

3·49

cR

Jan

1991

–Dec

199

10·

23f

211h

0·4

5P:

A:P

Tho

mso

n et

al.,

199

5

K

ular

i−

14·0

8, 1

3·40

cR

Jan

1991

–Dec

199

17·

65f

0·28

h7·

85

P:A

:PT

hom

son

et a

l., 1

995

M

adin

a−

15·2

5, 1

3·52

aR

NA

198

8–N

A 1

988

7·45

f23

76i

177·

05

100:

0:0

Lin

dsay

et a

l., 1

993

M

ale

Kun

da−

15·3

0, 1

3·55

bR

NA

198

8–N

A 1

988

2·60

f26

92i

70·0

510

0:0:

0L

inds

ay e

t al.,

199

3

N

iaw

odur

ulun

g−

15·2

2, 1

3·46

aR

NA

198

8–N

A 1

988

0·00

f14

81i

0·0

510

0:0:

0L

inds

ay e

t al.,

199

3

Pa

kali

Ba

−15

·25,

13·

50b

RN

A 1

988–

NA

198

83·

04 f

3253

i99

·05

100:

0:0

Lin

dsay

et a

l., 1

993

Sa

liken

e−

15·9

7, 1

3·48

cR

Jan

1991

–Dec

199

10·

55f

360h

1·9

5P:

A:P

Tho

mso

n et

al.,

199

5

Sa

re A

lpha

−13

·98,

13·

37b

RJa

n 19

91–D

ec 1

991

6·07

f18

7h11

·25

P:A

:PT

hom

son

et a

l., 1

995

Trans R Soc Trop Med Hyg. Author manuscript; available in PMC 2011 October 31.

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Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

Sa

ruja

−14

·90,

13·

55c

IJa

n 19

91–D

ec 1

991

2·17

f23

1h5·

05

P:A

:PT

hom

son

et a

l., 1

995

Sa

ruja

−14

·90,

13·

55c

IM

ar 1

987–

Jun

1988

NA

fN

Ai

3·0

kN

A10

0:0:

0L

inds

ay e

t al.,

199

1

Si

bano

r−

16·2

0, 1

3·21

bR

Jan

1991

–Dec

199

12·

88f

113h

3·2

5P:

A:P

Tho

mso

n et

al.,

199

4

Si

tahu

ma

−15

·40,

13·

43a

RN

A 1

988–

NA

198

82·

23 f

3366

i75

·05

100:

0:0

Lin

dsay

et a

l., 1

993

Su

tuko

ba−

14·0

2, 1

3·50

cR

Jan

1991

–Dec

199

12·

94f

34h

1·0

5P:

A:P

Tho

mso

n et

al.,

199

4

T

uran

−15

·72,

13·

58a

RJu

n 19

86–D

ec 1

986

2·70

e89

0i23

·83

100:

0:0

Lin

dsay

et a

l., 1

989

W

ellin

gara

Ba

−15

·26,

13·

41a

RN

A 1

988–

NA

198

82·

19 f

1553

i34

·05

100:

0:0

Lin

dsay

et a

l., 1

993

Ken

ya

A

hero

34·9

2, −

0·17

cI

May

198

9–Ju

n 19

90N

Af

NA

g41

6·0

715

:85:

0G

ithek

o et

al.,

199

3

Fu

mbi

ni39

·84,

−3·

61c

NA

Jan

1992

–May

199

32·

30 f

131g

3·0

195

:5:0

Mbo

go e

t al.,

199

5

K

ambi

ya

War

i39

·84,

−3·

52c

U/R

Jan

1992

–May

199

310

·54

f37

g3·

62

95:5

:0M

bogo

et a

l., 1

995

K

aoye

ni39

·90,

−3·

46c

NA

Jan

1992

–May

199

34·

08 f

61g

2·5

195

:5:0

Mbo

go e

t al.,

199

5

K

anya

weg

i34

·67,

−0·

92c

RJu

n 19

91–M

ay 1

992

5·29

f49

17gh

259·

9N

A64

:36:

0O

loo

et a

l., 1

996

K

arim

a37

·32,

−0·

69c

NA

Oct

198

6–Ju

n 19

872·

65 f

657

g17

·4N

A80

:10:

10Ij

umba

et a

l., 1

990

K

ibar

ani

39·8

5, −

3·58

cN

AJa

n 19

92–M

ay 1

993

11·3

1 f

159g

18·0

495

:5:0

Mbo

go e

t al.,

199

5

K

ilifi

Tow

n39

·85,

−3·

63b

UD

ec 1

990–

Nov

199

12·

17 f

69gh

1·5

210

0:0:

0M

bogo

et a

l., 1

993b

K

isia

n34

·67,

−0·

07b

RO

ct 1

985–

Jun

1988

5·98

e f

5001

g29

9·3

5–6

76:2

4:0

Bei

er e

t al.,

199

0

L

oboi

sw

amp

36·0

6, 0

·36a

RN

A2·

55 e

915

h23

·42

84:1

6:0

Ani

edu,

199

7

M

ikin

giri

ni39

·87,

−3·

56c

NA

Jun

1992

–May

199

30·

00 f

46g

0·0

00:

0:0

Mbo

go e

t al.,

199

5

M

iwan

i35

·01,

−0·

59c

RM

ay 1

989–

Jun

1990

NA

fN

Ag

91·0

380

:20:

0G

ithek

o et

al.,

199

3

M

tond

ia39

·90,

−3·

57c

NA

Jun

1992

–May

199

32·

09 f

2844

g59

·62

95:5

:0M

bogo

et a

l., 1

995

M

ukom

be39

·86,

−3·

52c

NA

Jun

1992

–May

199

37·

25 f

52g

3·8

295

:5:0

Mbo

go e

t al.,

199

5

M

umia

s34

·49,

0·1

8cR

May

199

5–M

ar 1

996

7·22

f64

7 h

46·7

763

:37:

0Sh

ililu

et a

l., 1

998

Pe

rker

ra ir

riga

tion

sche

me

35·9

7, 0

·47a

IN

A3·

08 e

533h

16·4

210

0:0:

0A

nied

u, 1

997

Sa

radi

di34

·38,

−0·

12a

RFe

b 19

86–0

ct 1

987

NA

efN

Ag

273·

85

90:1

0:0

Bei

er e

t al.,

199

4

Sa

radi

di34

·38,

−0·

12a

RO

ct 1

985–

Jun

1988

17·1

e f

1387

g23

7·3

590

:10:

0B

eier

et a

l., 1

990

So

koke

39·8

2, −

3·53

bN

AD

ec 1

990–

Nov

199

14·

23 f

189g

h8·

04

100:

0:0

Mbo

go e

t al.,

199

3b

Trans R Soc Trop Med Hyg. Author manuscript; available in PMC 2011 October 31.

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Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

U

fuon

i39

·93,

−3·

46c

NA

Jun

1992

–May

199

30·

01 f

19g

0·0

195

:5:0

Mbo

go e

t al.,

199

5

Z

ower

ani

39·9

2, −

3·51

cN

AJu

n 19

92–M

ay 1

993

2·35

f68

g1·

61

95:5

:0M

bogo

et a

l., 1

995

Mad

agas

car

A

mbo

difo

tatr

a, S

t Jos

eph,

Mar

oman

dia

49·9

0, −

17·0

0bR

Nov

198

8–0c

t 198

90·

59 f

1376

1 g

82·0

12P:

P:P

Font

enill

e et

al.,

199

2

M

anar

ints

oa47

·42,

−18

·92c

RO

ct 1

987–

Jul 1

988

0·71

f21

2 g

1·5

4–5

97:3

:0L

eper

s et

al.,

199

1

M

anar

ints

oa47

·42,

−18

·92c

RO

ct 1

988–

Feb

1990

0·14

f65

7 g

0·9

NA

NA

Font

enill

e et

al.,

199

0

Moz

ambi

que

M

atol

a32

·93,

−25

·94a

U/R

Jan

1994

–Jun

199

5N

Af

NA

g12

NA

P:P

:AT

hom

pson

et a

l., 1

997

Sene

gal

A

éré

Lao

−14

·30,

16·

40a

RM

ay 1

982–

Aug

198

30·

24 e

1600

g3·

83–

410

0:0:

0V

ercr

uyss

e, 1

985

A

ffin

iam

, Dia

gobe

l,

T

endi

man

e−

16·3

0, 1

2·70

aR

Jan

1985

–Nov

198

50·

03 e

2249

0 g

7·0

510

0:0:

0Fa

ye e

t al.,

199

4

B

arke

dji

−14

·87,

15·

28d

RJu

l 199

4–M

ar 1

996

NA

fN

Agh

111·

12–

310

0:0:

0L

e M

asso

n et

al.,

199

7

B

oké

Dia

llobé

−14

·00,

16·

10a

RM

ay 1

982–

Aug

198

31·

2 e

200g

2·4

3–4

100:

0:0

Ver

cruy

sse,

198

5

D

akar

, aro

und

Gra

nde

Nia

ye m

arsh

−17

·42,

14·

75d

NA

Jan

1988

–Dec

198

8N

Ae

NA

g0·

1N

A10

0:0:

0T

rape

et a

l., 1

992

D

ielm

o−

16·4

2, 1

3·72

dR

Apr

199

0–M

ar 1

992

1·29

f14

790g

191·

55

69:3

1:0

Kon

até

et a

l., 1

994

D

ielm

o−

16·4

2, 1

3·72

bR

Apr

199

2–M

ar 1

993

NA

fN

Agh

222·

86

23:7

7:0

Font

enill

e et

al.,

199

7b

D

ielm

o−

16·4

2, 1

3·72

bR

Apr

199

3–M

ar 1

994

NA

fN

Agh

78·5

4–5

74:2

6:0

Font

enill

e et

al.,

199

7b

D

ielm

o−

16·4

2, 1

3·72

bR

Apr

199

4–M

ar 1

995

NA

fN

Agh

135·

24

66:3

4:0

Font

enill

e et

al.,

199

7b

D

ielm

o−

16·4

2, 1

3·72

bR

Jan

1990

–Dec

199

0N

AN

A?

NA

NA

?11

5·0

410

0:0:

0R

ogie

r &

Tra

pe, 1

993

D

ielm

o−

16·4

2, 1

3·72

bR

Jun

1990

–May

199

11·

04e

9731

g10

1·2

4P:

P:A

Tra

pe e

t al.,

199

4

D

ielm

o−

16·4

2, 1

3·72

bR

Jun

1991

–May

199

21.

57e

1735

7 g

272·

56

P:P:

AT

rape

et a

l., 1

994

D

iohi

ne−

16·5

2, 1

4·50

bR

Jan

1995

–Dec

199

51·

95 f

680g

13·3

510

0:0:

0R

ober

t et a

l., 1

998

D

iom

ando

u D

ieri

−14

·44,

16·

50a

IJu

n 19

90–N

ov 1

991

0·00

e26

65g

0·0

00:

0:0

Faye

et a

l., 1

993

D

iom

ando

u W

alo

−14

·43,

16·

51a

IJu

n 19

90–N

ov 1

991

0·09

e59

13g

5·2

110

0:0:

0Fa

ye e

t al.,

199

3

K

assa

ck-N

ord

−16

·03,

16·

40a

RSe

p 19

92–N

ov 1

994

0·00

fN

Ag

0·0

00:

0:0

Faye

et a

l., 1

995b

K

otio

kh−

16·5

8, 1

4·48

aR

Jan

1995

–Dec

199

51·

75 f

1558

g27

·38

100:

0:0

Rob

ert e

t al.,

199

8

Trans R Soc Trop Med Hyg. Author manuscript; available in PMC 2011 October 31.

Europe PM

C Funders A

uthor Manuscripts

Europe PM

C Funders A

uthor Manuscripts

Hay et al. Page 23

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

M

aka-

Dia

ma

−16

·40,

16·

20a

RSe

p 19

92–N

ov 1

994

0·00

fN

Ag

0·0

00:

0:0

Faye

et a

l., 1

995b

N

diop

−16

·42,

13·

75b

RJa

n 19

93–D

ec 1

993

NA

fN

Ag

63·0

210

0:0:

0Fo

nten

ille

et a

l., 1

997a

N

diop

−16

·42,

13·

75b

RJa

n 19

94–D

ec 1

994

NA

fN

Ag

17·0

210

0:0:

0Fo

nten

ille

et a

l., 1

997a

N

diop

−16

·42,

13·

75b

RJa

n 19

95–D

ec 1

995

NA

fN

Ag

37·0

293

:7:0

*Fo

nten

ille

et a

l., 1

997a

N

diop

−16

·42,

13·

75b

RJa

n 19

96–D

ec 1

996

NA

fN

Ag

7·0

110

0:0:

0Fo

nten

ille

et a

l., 1

997a

N

diop

−16

·42,

13·

75b

RM

ay 1

993–

Dec

199

6N

Af

NA

g31

·02

98:2

:0Fo

nten

ille

et a

l., 1

997a

N

gayo

khem

e−

16·4

3, 1

4·53

bR

Jan

1995

–Dec

199

51·

80f

512g

9·2

NA

100:

0:0

Rob

ert e

t al.,

199

8

Po

ut r

egio

n−

17·0

7, 1

4·77

aN

AA

ug 1

988–

Jul 1

989

0·00

e23

908

g0·

00

0:0:

0Fa

ye, 1

992

Pi

kine

−17

·40,

14·

75b

UO

ct 1

979–

Dec

198

00·

55e

7818

g43

·04

100:

0:0

Ver

cruy

sse

& J

ancl

oes,

1981

T

hiay

e, N

gadi

aga,

D

iam

ballo

−17

·05,

14·

95a

RJu

l 199

1–Ju

n 19

920·

48f

2305

g11

·04

100:

0:0

Faye

et a

l0, 1

995a

T

akèm

e an

d O

usse

uk−

16·2

0, 1

2·80

aN

AJa

n 19

85–N

ov 1

985

0·36

e15

123

g55

·05

100:

0:0

Faye

et a

l., 1

994

T

ould

e G

alle

−14

·60,

16·

53a

IJu

n 19

90–N

ov 1

991

0·00

e43

8g0·

00

0:0:

0Fa

ye e

t al.,

199

3

Sier

ra L

eone

B

ayam

a−

11·7

7, 8

·00a

RN

ov 1

990–

Oct

199

14·

36 f

2029

4 g

884·

27

100:

0:0

Boc

kari

e et

al.,

199

5

B

ayam

a−

11·7

7, 8

·00a

RN

ov 1

990–

Oct

199

13·

90f

2073

2g80

8·5

1210

0:0:

0B

ocka

rie

et a

l., 1

993

B

ayam

a−

11·7

7, 8

·00a

RA

ug 1

993–

Nov

199

46·

82f

6125

g41

7·6

NA

NA

E. B

. Mag

bity

, 199

9, p

ers.

com

.; M

agbi

ty e

t al.,

199

9

B

aom

a−

11·7

3, 8

·04a

RA

ug 1

993–

Nov

199

42·

16f

3924

g84

·8N

AN

AE

. B. M

agbi

ty, 1

999,

per

s.co

m.;

Mag

bity

et a

l., 1

999

D

anda

bu−

11·6

4, 8

·15a

RA

ug 1

993–

Nov

199

45·

38f

1507

g81

·1N

AN

AE

. B. M

agbi

ty, 1

999,

per

s,co

m.;

Mag

bity

et a

l., 1

999

G

umah

un−

11·5

0, 8

·18a

RJu

n 19

92–J

ul 1

993

6·94

f17

5gi

12·1

NA

100:

0:0

Mag

bity

et a

l., 1

997;

E. B

. Mag

bity

, 199

9,pe

rs. c

om.

Ja

iam

a−

11·6

9, 8

·16a

RA

ug 1

993–

Nov

199

48·

72f

2602

g22

6·9

NA

NA

E. B

.Mag

bity

, 199

9, p

ers.

com

.; M

agbi

ty e

t al.,

199

9

K

onjo

dorm

a−

11·5

0, 8

·15a

RJu

n 19

92–J

ul 1

993

3·96

f81

8gj

32·4

NA

100:

0:0

Mag

bity

et a

l., 1

997;

E. B

. Mag

bity

, 199

9,pe

rs. c

om.

K

pete

ma

−11

·50,

8·1

3aR

Jun

1992

–Jul

199

38·

81f

1551

gj13

6·7

NA

100:

0:0

Mag

bity

et a

l., 1

997;

E. B

. Mag

bity

, 199

9,pe

rs. c

om.

M

anja

ma

−11

·74,

8·0

2aR

Aug

199

3–N

ov 1

994

12·1

3f23

40g

283·

7N

AN

AE

. B. M

agbi

ty, 1

999,

per

s.co

m.;

Mag

bity

et a

l., 1

999

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Hay et al. Page 24

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

M

ende

wa

−11

·48,

8·1

6aR

Jun

1992

–Jul

199

34·

74f

128g

j6·

1N

A10

0:0:

0M

agbi

ty e

t al.,

199

7;E

. B. M

agbi

ty, 1

999,

pers

. com

.

M

ende

wa

−11

·48,

8·1

6bR

Jan

1990

–Apr

199

1N

Af

NA

NA

21·9

4–5

58:4

2:0

Boc

kari

e et

al.,

199

4

N

engb

ema

−11

·68,

8·1

3aR

Jun

1992

–Jul

199

34·

42f

471g

j20

·8N

A10

0:0:

0M

agbi

ty e

t al.,

199

7;E

. B. M

agbi

ty, 1

999,

pers

. com

.

N

engb

ema

−11

·68,

8·1

3aR

Jan

1990

–Apr

199

1N

NN

AN

A21

·54–

597

:3:0

Boc

kari

e et

al.,

199

4

N

galu

−11

·56,

8·1

1aR

Jun

1992

–Jul

199

36·

08f

712g

j43

·3N

A10

0:0:

0M

agbi

ty e

t al.,

199

7;E

. B. M

agbi

ty, 1

999,

pers

. com

.

N

jala

-Kom

boya

−11

·54,

8·2

0aR

Jan

1990

–Apr

199

1N

Af

NA

NA

26·7

4–5

96:4

:0B

ocka

rie

et a

l., 1

994

N

yand

eyam

a−

11·6

6, 8

·12a

RJu

n 19

92–J

ul 1

993

4·05

f99

3gj

40·2

NA

100:

0:0

Mag

bity

et a

l., 1

997;

E. B

. Mag

bity

, 199

9,pe

rs. c

om.

N

yand

eyam

a−

11·6

6, 8

·12a

RJa

n 19

90–A

pr 1

991

NA

fN

AN

A35

·54–

597

:3:0

Boc

kari

e et

al.,

199

4

T

ondo

ya−

11·6

4, 8

·13a

RJu

n 19

92–J

ul 1

993

7·30

f14

24gj

102.

0N

A10

0:0:

0M

agbi

ty e

t al.,

199

7;E

. B. M

agbi

ty, 1

999,

pers

. com

.

Tan

zani

a

C

hasi

mba

38·8

2, −

6·58

cR

Jan

1992

–Dec

199

2N

Af

NA

i21

7·7

987

:13:

0Sh

iff

et a

l., 1

995

Id

ete

36·4

8, −

8·10

bR

Jan

1992

–Dec

199

4N

Af

NA

i58

4·0

12P:

P:A

Cha

rlw

ood

et a

l., 1

998

K

ongo

38·8

3, −

6·53

bR

Jan

1992

–Dec

199

2N

Af

NA

i57

6·7

1281

:19:

0Sh

iff

et a

l., 1

995

K

aole

38·9

3, −

6·45

cR

Jan

1996

–Dec

199

6N

Af

NA

i12

4·3

1266

:34:

0T

emu

et a

l., 1

998

K

ereg

e39

·03,

−6·

57b

RJa

n 19

92–D

ec 1

992

NA

fN

Ai

271·

611

88:1

2:0

Shif

f et

al.,

199

5

K

ikw

awila

36·7

5, −

8·08

aR

Dec

198

3–A

ug 1

984

2·49

e11

427

NA

284·

03

69:3

1:0

Bir

o, 1

987

K

ikw

azu

38·8

2, −

5·40

aR

Apr

198

8–D

ec 1

989

NA

eN

Ai

667·

03

100:

0:0

Mnz

ava,

199

1

K

ongo

38·8

3, −

6·53

cR

Jan

1996

–Dec

199

6N

Af

NA

i30

6·3

1283

:17:

0T

emu

et a

l., 1

998

K

umba

mto

ni38

·76,

−5·

10a

RJa

n 19

87–D

ec 1

988

7·14

f60

04i

428·

8N

AP

:P:P

Mag

esa

et a

l., 1

991

K

umba

mto

ni38

·82,

−5·

31a

RA

pr 1

987–

Mar

198

9N

Ae

NA

i42

0·0

610

0:0:

0M

nzav

a, 1

991

M

apin

ga39

·07,

−6·

60b

RJa

n 19

92–D

ec 1

992

NA

fN

Ai

235·

69

83:1

7:0

Shif

f et

al.,

199

5

M

atim

bwa

38·8

7, −

6·50

bR

Jan

1992

–Dec

199

2N

Af

NA

i70

2·6

1290

:10:

0Sh

iff

et a

l., 1

995

M

atim

bwa

38·8

7, −

6·50

cR

Jan

1996

–Dec

199

6N

Af

NA

i12

2·1

1251

:49:

0T

emu

et a

l., 1

998

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Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-us

e2St

udy

date

Spor

ozoi

te

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

M

iche

nga

36·6

3, −

8·12

aR

Jan

1990

–Dec

199

0N

Ae

NA

i54

7·5

410

0:N

A:N

AB

abik

er e

t al.,

199

7

M

iche

nga

36·6

3, −

8·12

aR

Jan

1990

–Dec

199

1N

Af

NA

i54

8·0

410

0:N

A:N

AL

yim

o, 1

993

N

amaw

ala

36·4

0, −

8·15

eR

Mar

199

0–Ju

l 199

11.

37 f

2409

0i32

9·0

6P:

P:A

Smith

et a

l., 1

993

T

emgi

ni a

nd E

nzi

38·7

6, −

5·18

cN

AN

A 1

995–

NA

199

6N

Af

NA

gi40

5·0

NA

NA

C. F

. Cur

tis, 1

998,

pers

. com

.

U

mba

38·8

7, −

5,17

aR

Jan

1987

–Dec

198

84.

68 f

1189

9i55

6·7

NA

P:P

:PM

ages

a et

al.,

199

1

Y

ombo

38·8

5, −

6·57

bR

Jan

1992

–Dec

199

2N

Af

NA

i22

0·6

1079

:21:

0Sh

iff

et a

l., 1

995

Z

inga

38·9

8, −

6·52

bR

Jan

1992

–Dec

199

2N

Af

NA

i93

·77

88:1

2:0

Shif

f et

al.,

199

5

1 Sour

ces

of la

titud

e/lo

ngitu

de:

a publ

ishe

d m

aps

b Geo

Nam

e™ d

igita

l gaz

ette

er C

D-R

OM

;

c corr

espo

nden

ce w

ith a

utho

rs;

d cite

d in

the

refe

renc

e.

2 R, r

ural

; U, u

rban

; I, i

rrig

ated

ric

e.

3 Spor

ozoi

te d

etec

tion

met

hod:

e diss

ectio

n;

f EL

ISA

.

4 ma

sam

plin

g te

chni

que:

g hum

an b

ait;

h inse

ctic

ide

spra

y;

i i lig

ht tr

aps;

j exit

trap

s.

5 EIR

val

ues:

k conv

erte

d us

ing

(Por

t et a

l., 1

980)

ave

rage

chi

ld-t

o-ad

ult c

onve

rsio

n fa

ctor

, f, o

f 3·

57.

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Hay et al. Page 266 V

alue

s in

ital

ics

reco

rd th

e nu

mbe

r of

mon

ths

in w

hich

75%

of

tran

smis

sion

occ

urs.

Oth

er v

alue

s re

cord

the

leng

th o

f th

e en

tire

tran

smis

sion

sea

son.

7 For

Ano

phel

es g

arnb

iae

s.l.:

An.

fune

stus

: any

oth

er lo

cally

impo

rtan

t vec

tor.

Whe

re a

bsol

ute

valu

es a

re u

nava

ilabl

e P

indi

cate

s pr

esen

ce o

nly

and

A a

bsen

ce.

NA

ref

ers

to d

ata

that

wer

e no

t ava

ilabl

e, o

r no

t app

licab

le. V

alue

s in

bol

d re

fer

to c

alcu

late

d va

lues

.

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Tabl

e 2

Loc

atio

ns in

Afr

ica

for

whi

ch a

nnua

l EIR

dat

a w

ere

publ

ishe

d th

at c

ould

not

be

geo-

refe

renc

ed

Cou

ntry

and

sit

eL

ocat

ion1

(Lon

g., L

at.)

Lan

d-

use2

Stud

y da

teSp

oroz

oite

inde

x3 (

%)

Bit

ing

rate

4(m

a an

nual

)E

IR5

(ann

ual)

Seas

onal

ity6

(mon

ths)

Rel

ativ

e E

IRtr

ansm

issi

on b

y

spec

ies7

(%

)

Cit

atio

n

Cam

eroo

n

Y

aoun

dé, N

ikol

Bis

son

NA

, NA

RM

ar 1

989–

Mar

199

01·

67e

1814

g30

·33

100:

0:0

Fond

jo e

t al.,

199

2

Con

go, D

emoc

ratic

Rep

ublic

of

M

bang

u-m

bam

uN

A, N

AR

Feb

1990

–Nov

199

02·

50e

17·3

g15

7·0

1210

0:0:

0K

arch

et a

l., 1

993

M

bans

ale

NA

, NA

RFe

b 19

90–N

ov 1

990

3·50

e50

01g

175·

212

100:

0:0

Kar

ch e

t al.,

199

3

M

bans

alé

NA

, NA

RFe

b 19

91–N

ov 1

991

4·80

e68

26g

324·

912

100:

0:0

Kar

ch e

t al.,

199

3

Côt

e d’

Ivoi

re

B

ouak

é, m

arke

t gar

den

dist

rict

sN

A, N

AR

Jan

1992

–Dec

199

22·

01 N

A43

80g

888

100:

0:0

Dos

sou-

yovo

et a

l., 1

994

B

ouak

é, r

ice

fiel

ds d

istr

ict

NA

, NA

IJa

n 19

92–D

ec 1

992

0–68

NA

1861

5g12

69

100:

0:0

Dos

sou-

yovo

et a

l., 1

994

Egy

pt

A

bhee

t vill

age

NA

, NA

RFe

b 19

83–F

eb 1

984

0·59

e30

8g1·

81

0:0:

100

El S

aid

et a

l., 1

986

Suda

n

A

sar

NA

, NA

RO

ct 1

990–

Dec

199

02·

06e

NA

ih0·

6N

A10

0:0:

0B

abik

er e

t al.,

199

7

1 Sour

ces

of la

titud

e/lo

ngitu

de:

a publ

ishe

d m

aps;

b Geo

Nam

e™di

gita

l gaz

ette

er C

D–R

OM

;

c corr

espo

nden

ce w

ith a

utho

rs;

d cite

d in

the

refe

renc

e.

2 R, r

ural

; U, u

rban

; I, i

rrig

ated

ric

e.

3 Spor

ozoi

te d

etec

tion

met

hod:

e diss

ectio

n;

f EL

ISA

.

4 ma

sam

plin

g te

chni

que:

Trans R Soc Trop Med Hyg. Author manuscript; available in PMC 2011 October 31.

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Hay et al. Page 28g hu

man

bai

t;

h inse

ctic

ide

spra

y;

i light

trap

s;

j exit

trap

s.

5 EIR

val

ues:

k conv

erte

d us

ing

(Por

t et a

l., 1

980)

ave

rage

chi

ld–t

o–ad

ult c

onve

rsio

n fa

ctor

, f, o

f 3·

57.

6 Val

ues

in it

alic

s re

cord

the

num

ber

of m

onth

s in

whi

ch 7

5% o

f tr

ansm

issi

on o

ccur

s. O

ther

val

ues

reco

rd th

e le

ngth

of

the

entir

e tr

ansm

issi

on s

easo

n.

7 For

Ano

phel

es g

ambi

ae s

.l.: A

n. fu

nest

us: a

ny o

ther

loca

lly im

port

ant v

ecto

r. W

here

abs

olut

e va

lues

are

una

vaila

ble

P in

dica

tes

pres

ence

onl

y an

d A

abs

ence

.

NA

ref

ers

to d

ata

that

wer

e no

t ava

ilabl

e, o

r no

t app

licab

le. V

alue

s in

bol

d re

fer

to c

alcu

late

d va

lues

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Hay et al. Page 29

Tabl

e 3

Var

ianc

e in

EIR

val

ues

with

in c

ount

ries

for

all

spat

ially

uni

que

rura

l site

s (1

33 s

ites

tota

l with

tem

pora

l dup

licat

es a

vera

ged)

Bur

kina

Fas

oK

enya

Sene

gal

Sier

raL

eone

Tan

zani

aG

ambi

a,T

heA

llA

fric

a

Mea

n115

6·8

64·3

28·7

129·

036

7·0

42·1

134·

2

Med

ian

133

17·4

9·2

62·2

405

1176

·7

Max

imum

441·

629

9·3

159·

570

3·4

667

177

703·

4

Min

imum

550

012

·193

·70

0

Ran

ge38

6·6

299·

315

9·5

691·

357

3·3

177

703·

4

Stan

dard

dev

iatio

n96

·510

2·3

46·8

184·

516

4·6

52·3

162·

2

Stan

dard

err

or o

f m

ean

24·9

24·8

12·1

49·3

39·9

12·7

14·1

Var

iatio

n15

·938

·642

·038

·210

·930

·110

·5

Num

ber

of s

ites

1517

1514

1717

133

1 The

ari

thm

etic

mea

n is

use

d as

a m

easu

re o

f ce

ntra

l ten

denc

y in

the

data

(D

osso

u-Y

ovo

et a

l., 1

994)

. Med

ian

valu

es a

re a

lso

pres

ente

d as

they

are

less

sen

sitiv

e to

non

-nor

mal

dis

trib

utio

ns.

Trans R Soc Trop Med Hyg. Author manuscript; available in PMC 2011 October 31.